Opinion

Coral bleaching: the role of the host

Andrew H. Baird1, Ranjeet Bhagooli2, Peter J. Ralph3 and Shunichi Takahashi4
1

ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia
Department of Biosciences, University of Mauritius, Reduit, Mauritius
3
Institute for Water and Environmental Resource Management, Department of Environmental Sciences, University of Technology
Sydney, Broadway, NSW 2007, Australia
4
Molecular Plant Physiology Group, Research School of Biological Sciences, The Australian National University, Canberra, ACT
0200, Australia
2

Coral bleaching caused by global warming is one of the

major threats to coral reefs. Very recently, research has
focused on the possibility of corals switching symbionts
as a means of adjusting to accelerating increases in sea
surface temperature. Although symbionts are clearly of
fundamental importance, many aspects of coral bleaching cannot be readily explained by differences in symbionts among coral species. Here we outline several
potential mechanisms by which the host might influence
the bleaching response, and conclude that predicting the
fate of corals in response to climate change requires
both members of the symbiosis to be considered
equally.
Reefs under threat from global warming
Coral reefs are under severe threat from many sources,
including mass coral mortality events caused largely by sea
surface temperature (SST) anomalies associated with global warming [1]. Corals are a symbiosis between the
animal host and micro-algae from the genus Symbiodinium. Under stress, such as elevated SST, the algal endosymbionts are expelled, a process that is known as coral
bleaching. Projected increases in SST caused by global
warming have led some authorities to predict that reefs
might disappear entirely within 2050 years [2]. However,
this prediction is based largely on the assumption that
corals will not be able to adapt to accelerating rates of
environmental change [3] (Box 1). One mechanism that
might allow corals to rapidly adjust to the projected rises in
SST is for the host to switch to a more thermally tolerant
symbiotic partner [4]. This mechanism has received considerable attention in the recent literature; however,
experimental support remains inconclusive [57]. One
positive result of this recent focus on the role of the
symbiont has been a rapid increase in physiological
research, and significant progress has been made toward
understanding the mechanisms of bleaching (see next
section). Unfortunately, there has yet to be a parallel
increase in ecological research to explore the consequences
of bleaching, particularly at the population level, possibly
because the role of the host in influencing its fate is less
well recognised. Here we outline evidence for a role of the
host in determining a corals bleaching response and propose several potential mechanisms to explain this role. We
conclude that an understanding of the threat climate
Corresponding author: Baird, A.H. (andrew.baird@jcu.edu.au).

16

change poses to reef corals will remain incomplete unless

both members of the symbiosis are considered equally. We
argue that the holobiont (the animal and symbiont in
combination) is the relevant unit of selection and therefore
the appropriate target for the research required to determine the capacity of coral to respond to changing climate.
The photoinhibition model of coral bleaching
The recent emphasis on the role of the symbiont in thermal
tolerance is justified by the finding that thermal bleaching
begins with an accumulation of oxidative stress at photosystem II (PSII) in the symbiont, a process known as
photoinhibition [8]. Because photoinhibition sensitivity
to increased temperature varies among Symbiodinium
clades, differences in sensitivity among corals are determined, in some species, by the symbiont [9,10]. However,
the response of the holobiont is not always related to
differences in the thermal tolerance of the symbiont. For
example, coral species vary considerably in their response
to thermal stress [11]. Some genera, such as Stylophora,
Pocillopora and Acropora, are highly susceptible to bleaching, whereas Cyphastrea, Goniopora, Galaxea and Pavona
are highly resistant, and this hierarchy of susceptibility is
consistent over a wide geographic scale [12]. However,
these differences in susceptibility among species are not
caused by species hosting different types of symbionts. In
particular, some common Symbiodinium types, such as C1
and C3, occur in many different host species with a divergent response to temperature, including the highly
susceptible Seriatopora hystrix, and many taxa recognised
as resilient to thermal stress, including Favia, Goniastrea
and Platygyra [13]. Furthermore, the production of reactive oxygen species (ROS) in cells is a common early event
in response to many types of stress and is not unique to
photosynthetic organisms (Figure 1). Indeed, physiological
changes in the host, such as reduced thickness of the
epidermis and apoptosis of gastrodermal cells, might
precede changes in symbionts when corals are exposed
to heat [14]. Although the evidence for a primary role of
the symbiont in coral bleaching is overwhelming, there are,
nonetheless, many ways in which the host can limit the
level of damage sustained by the symbionts, and thus
influence the response of the holobiont.
Paradoxically, light is both the driving force of photosynthesis and the cause of photodamage to the photosynthetic machinery, primarily PSII. Photodamaged PSII is
rapidly and efficiently repaired through the replacement of

0169-5347/$ see front matter 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.09.005 Available online 18 November 2008

Opinion
Box 1. Coral bleaching and rates of adaptation
The prediction that reefs might disappear as a result of global
warming is based largely on the assertion that rates of environmental change are too rapid for corals to adjust before they
succumb to high temperature [3]. Two key assumptions underlie
such predictions: corals have comparatively long generation times
and gene flow is too great for local adaptation. How correct are
these assumptions?
Many features of coral life histories, such as extended life spans,
delayed maturation and colony fission, should result in long
generation times [49]. In species with these traits, generation times
are between 33 and 37 years [50]. However, other corals, in
particular those species most susceptible to thermal stress such as
many species of Acropora and Pocillopora, mature early, grow
rapidly and suffer whole-colony mortality, as opposed to colony
fission, following mechanical disturbances and thermal stress [51].
The life histories of these ecologically important and abundant
species suggest an as-yet undefined and underappreciated capacity
to adapt rapidly to changing environments.
Furthermore, the assumption that the scale of dispersal is too large
to allow for adaptation to local environments might also be incorrect.
The relationship between the supply of propagules and larval
recruitment suggests that the majority of recruits are likely to be of
local origin [52], and this is further supported by experiments which
demonstrate that settlement is very rapid in some species [53].
Genetic studies also indicate that populations of many species are
highly subdivided, which is indicative of restricted gene flow [54].
The major appeal of the adaptive bleaching hypothesis [4] is that
it offers a mechanism enabling adjustment to stress over the course
of weeks, as opposed to generations. However, evolution by natural
selection can occur rapidly in some situations [55], and therefore
novel mechanisms, such as switching symbionts, might not be
required for corals to adjust to climate change.

photodamaged proteins with newly synthesised proteins

[15]. Thus, photoinhibition occurs only when the rate of
photodamage to PSII exceeds the rate of its repair. A
moderate increase in temperature accelerates photoinhibition, primarily through inhibition of the repair process
[16,17]. However, the primary site of thermal stress is still
unresolved, with various authors arguing it is PSII [8], the

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Vol.24 No.1

thylakoid membrane [18] and/or the Calvin cycle [19].

Recent experimental evidence has demonstrated that
photodamage to PSII occurs in two steps: the primary
damage occurs in the oxygen-evolving complex of PSII
caused by ultraviolet radiation (UV) and strong blue light
(and less effectively by other visible light), whereas secondary damage is caused by light absorbed by photosynthetic pigments in the reaction centre of PSII [20].
Consequently, any mechanism that reduces UV and visible
light flux to symbiotic cells will potentially prevent photodamage and therefore might prevent photoinhibition-dependent coral bleaching (Figure 2).
Hypothetical mechanisms by which the host might
reduce bleaching damage
The coral host has several potential ways to reduce UV and
light flux to symbionts, including the production of fluorescent pigments (FP) and the acquisition of mycosporinelike amino acids (MAA). Similarly, the host has several
antioxidant systems and stress enzymes to deal with oxygen stress originating in the animal cell. Differences
among host species in their capacity to utilise these mechanisms might therefore determine differences among
species in response to stress.
Fluorescent pigments
The coral host produces a range of FPs belonging to a single
family of proteins, closely related to the green fluorescent
proteins [21]. FPs are highly abundant on reefs; up to 97%
of corals in shallow water on the Great Barrier Reef contain
fluorescent pigments [22,23]. By absorbing, scattering and
dissipating high-energy solar radiation via fluorescence,
FPs reduce photoinhibition and the severity of bleaching
damage to corals [23,24]. Many aspects of bleaching appear
to be related to differences in the abundance of FPs. For
example, bleaching-susceptible taxa, such as pocilloporids

Figure 1. A generalised sequence of stress. Stress was originally defined as a nonspecific response independent of the cause of stress [46]. For example, corals bleach in
response to high temperature, high light or high salinity and so forth, and therefore bleaching can be considered a stress response. In most stress responses, the production
of reactive oxygen species (ROS) in cells is a common early event. Superoxide is the most commonly produced ROS. Hydrogen peroxide (H2O2), which is the only diffusive
ROS molecule, is produced secondarily. In animal cells, ROS production is associated with the mitochondria; in photosynthetic organisms, it is also associated with the
chloroplasts [27]. Potentially toxic ROS are removed by antioxidant systems, which include enzymatic antioxidants such as superoxide dismutase and catalase, ascorbic
acid, carotenoids [27], FPs [47] and mycosporine glycine [28]. As long as these scavenging mechanisms are functional, ROS will not accumulate. Under severe stress,
however, these antioxidant systems might not be able to destroy all ROS produced, in which case oxidative damage will occur, leading to metabolic dysfunction, cell
destruction or mutation. In addition to antioxidant systems, there are repair systems to remove damaged molecules and to replace them with new ones. In this context,
antioxidant systems function as the primary line of defence and the repair systems act as a secondary line of defence against oxidative stress. If these mechanisms cannot
limit or suppress stress damage, living organisms will eventually die.

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Opinion

Trends in Ecology and Evolution Vol.24 No.1

Figure 2. The role of the coral host in preventing bleaching caused by moderate heat stress. Moderate heat (i) accelerates the production of hydrogen peroxide (H2O2) in the
chloroplasts of the algal symbionts either by damaging the thylakoid membrane or disrupting the Calvin cycle. H2O2 can spread from here to the host cell, where it activates
a cellular cascade akin to an innate immune response, which results in expulsion of symbionts (ii) [38]. The potential to scavenge H2O2 (iii) varies among host species and,
therefore, might influence difference in susceptibility to H2O2-dependent coral bleaching. In addition, H2O2 inhibits the repair of photodamage in PSII (iv), causing an
acceleration of photoinhibition and photobleaching of pigments in symbionts [48]. Finally, by accumulating UV-absorbing compounds, such as MAAs and FPs, the host can
intercept UV light (v), thereby limiting photodamage to PSII and preventing light-dependent coral bleaching (vi).

and acroporids, have relatively low densities of FPs,

whereas poritids, faviids and other less-susceptible taxa
have relatively high densities of FPs [22]. Similarly, highly
fluorescent colonies suffer less partial mortality following
bleaching than weakly fluorescent conspecifics [24].
Although the support for a role of FPs in reducing bleaching damage is compelling, a direct role of FPs in preventing
bleaching, for example by providing photoprotection,
remains to be tested experimentally. Furthermore, it is
not known whether FPs can provide relief from heat stress
alone.
Mycosporine-like amino acids
MAAs absorb UV and dissipate UV energy as heat without
forming toxic intermediates [25]. MAAs are synthesised
via the shikimic acid pathway and, because animals lack
this pathway, symbionts are presumed to be the source of
MAAs in corals [25]. Alternatively, they are acquired via
heterotrophic feeding. Whatever the source of these compounds, MAAs are far more abundant in host tissues than
in freshly isolated symbionts [25]. In addition, the diversity
of MAAs found in holobionts is far greater than that found
in Symbiodinium in isolation [25]. Whether this results
from the host stimulating symbionts to produce a greater
diversity of MAAs in hospite or because the host can modify
MAAs translocated from the symbiont remains unknown
[26]. However, it is clear that the host has a major influence
on the complement and distribution of MAAs in the holobiont, thereby moderating the amount of UV that reaches
symbiont cells and, thus, we hypothesise, influencing the
amount of damage sustained by symbionts.
Antioxidant systems
A similarly complex interplay between host and symbiont
is evident in response to oxidative stress. Potentially toxic
ROS caused by stress are removed by antioxidant systems,
which include enzymatic antioxidants such as superoxide
dismutase (SOD) and catalase, ascorbic acid, carotenoids
(reviewed in Ref. [27]) and mycosporine glycine [28]. Symbiotic hosts, such as the coral Stylophora pistillata and the
18

anemone Anemonia viridis, have many different types of

SOD, some of which are not found in non-symbiotic
animals, and these act in combination with the antioxidant
defences [28] of the symbiont to minimise oxidative
damage [29]. In particular, more types of SOD are active
in symbionts in isolation than when in hospite, indicating
that protective mechanisms of the host limit oxidative
damage sustained by the symbionts [29].
Heat-shock proteins
Stress proteins, such as the ubiquitous heat-shock proteins
(HSP), are another way that organisms cope with stress,
including temperature and high light. HSPs act as molecular chaperones, which maintain protein structure and
cell function, particularly following stress. Many different
HSPs are found in coral tissue and their activity influences
the bleaching response. For example, high-light-acclimatised tissues of the coral Goniastrea aspera have higher
concentrations of HSPs and these tissues do not bleach,
unlike areas of the same colony that had not acclimatised
to high light [30]. Importantly, neither the clade of symbiont nor algal antioxidant defences varied within colonies,
highlighting the role of host tissue in the bleaching
response of these colonies [30].
Change in diet in response to bleaching stress
Whereas much of the energy required for coral metabolism
is derived from Symbiodinium, many corals are also effective carnivores. Species which can increase carnivory survive experimental bleaching better than species which
cannot [31], presumably because the host can compensate
for the loss of energy caused by reduced densities of symbionts by increased heterotrophic feeding. Alternatively,
by increasing heterotrophic feeding, the hosts demands on
the symbiont might be reduced, allowing the symbiont to
allocate more energy to its own antioxidant defences and
potentially limiting damage to the algal cell. Nonetheless,
changes in the transfer of photosynthetic products from the
symbiont to the host in response to stress have yet to be
explored.

Opinion
Coral bleaching: a communication breakdown under
stress
Coral bleaching presents biologists with many conundrums. For example, many corals bleach at 12 8C above
historical mean summer maximum sea temperatures,
although the bleaching threshold might be modified by
ambient light levels. Whereas the actual temperature
threshold depends upon location, at most locations mass
bleaching thresholds are in the range of 2932 8C, which is
a surprisingly low temperature for tropical organisms to
suffer high mortality. Indeed, it is only symbiotic organisms, including corals, sea anemones, zoanthids and
sponges, that die during thermal anomalies [32]. Macroalgae do not bleach or die during coral mass bleaching
events, and photosynthesis in free-living micro-algae is
mostly unaffected below 35 8C [33]. Similarly, the critical
thermal maximum for tropical fish is between 34.7 8C and
40.0 8C [34]. Does living together present unique problems,
particularly when life becomes stressful?
Perhaps the bleaching phenomenon is best perceived
as a breakdown in communication. Under normal conditions, symbiosis is presumably maintained by the
release of signalling compounds from the symbiont
[35]. The host-derived symbiosome membrane might
mediate this signal transduction, although the role of
membrane components in interpartner communication
remains to be fully explored [36,37]. When the condition
of the symbiont is compromised under stress, signalling
is disrupted and the animal host defends itself, by expelling the symbiont or killing the animal cells that contain
symbionts [38,39]. Alternatively, bleaching might be the
result of a breakdown in the hosts normal processes of
population regulation of the symbiont at high temperature. Densities of Symbiodinium in coral cells are generally low and stable [40], despite the fact that the
potential population growth rate of symbiont cells is
much higher than host cells [41]. The host must, therefore, have mechanisms that regulate symbiont densities,
for example host factors that limit symbiont cell
division [42] or are potentially toxic to Symbiodinium
cells [43]. Other host regulatory mechanisms include
limiting the supply of essential nutrients to symbionts
[41] or digesting or expelling symbionts [43]. At nonstressful temperatures, the majority of symbionts
released are morphologically degraded and have low
photosynthetic efficiency [44]. By contrast, at stressful
temperatures, the majority of released symbionts appear
healthy [45] and photosynthetically active [44]. This
suggests that under stress, the coral hosts ability to
discriminate between healthy and underperforming symbionts is diminished. Whatever the details of this
relationship, living together clearly presents the organism with unique challenges, particularly when under
stress. Bleaching is clearly an emergent property of
the holobiont, the consequences of which cannot be fully
resolved when considering either partner in isolation.
Conclusions
Corals have been in symbiosis with photosynthetic organisms for up to 200 million years, a selective pressure that
has modified both host and symbiont [26,35]. Many fea-

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tures of the symbiosis, such as oxidative defences, MAA

abundance and symbiont density per cell, are the result of
complex molecular interactions between the partners. As
outlined above, there is abundant evidence that both partners are involved in determining the organisms response
to stress and, therefore, understanding the threat climate
change poses requires the organism to be treated as a
whole. In particular, population ecological studies of corals
are lacking and, consequently, the effects of temperature
on even the most basic vital rates in corals, such as growth,
mortality and fecundity, are largely unknown. To effectively address the issue of rates of adaptation in corals, and
whether or not they will be exceeded by rates of environmental change, long-term demographic studies are
required to detect temporal trends in life-history traits
and to explore the sensitivity of population growth to these
changes. The past ten years have seen great progress made
by physiologists and molecular biologists toward understanding the mechanism of coral bleaching. Now it is time
for ecologists to match this progress with studies designed
to determine the consequences of coral bleaching for coral
demography and, furthermore, to predict how climateinduced changes in coral demography will influence the
future of coral reefs.
Acknowledgements
Line Bay, Ross Hill, Bill Leggat and six anonymous reviewers provided
valuable comments on the article. Figure 1 was produced by Hideo
Yamasaki.

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